• cryptic species;
  • DNA;
  • ecology;
  • generalist;
  • molecular markers;
  • niche;
  • specialist


  1. Top of page
  2. Abstract

Most organisms represent specialized forms that arose as a result of natural selection and genetic drift to occupy distinct ecological niches. In animals, this process of specialization includes the behaviour of the organisms concerned, honed by locally-induced adaptations to specific host food plants (in herbivores) or prey items (in predators and parasitoids), and possibly reinforced by kairomones, including sex pheromones. The major thrust of evolution is towards ecological specialization as a result of the direct effects of intra- and interspecific competition. Adaptation to new resources lowers such competition and allows survival in new habitats/niches. Other benefits of food resource/habitat switching include ‘enemy free space’. If specialism is the norm for the vast majority of species, what of so-called generalists and generalism, which are widely used terms, but perhaps wrongly so? Does generalism exist or is it a mirage that disappears the closer that it is inspected? We review some of the aspects of specialism and generalism and argue that even apparent generalists are filling distinct ecological niches. Often, generalists are rather specific in terms of food preferences, although they may nevertheless remain opportunistic with an overall broad niche/resource width. When apparent ‘good’ species are examined using molecular (DNA) markers, they are often found to comprise cryptic species. Many generalists may be of this kind. If so, generalism warrants additional investigation to establish its scope and credentials. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 1–18.

‘To each his own.’

(Suum Cuique)

Cicero, Roman author, orator, and politician (106 BC to 43 BC)


  1. Top of page
  2. Abstract

According to the dictionary (OED; Simpson, 2000), ‘species’ is Latin for ‘appearance, form or kind’ and a ‘specie’ is a coin. The term ‘special’ and ‘specialization’ come from the same root. As a coin is the unit of currency, so a species is the unit of the speciation process (Claridge, Dawah & Wilson, 1997). Similar to coins, one ‘specie’ can be converted to another but, in the natural world, this can only come about by the processes of evolution involving natural selection and genetic drift (Claridge et al., 1997; Loxdale, Claridge & Mallet, 2010) and perhaps via induced epigenetic factors too (e.g. wing induction in aphids caused by crowding or predator/wasp parasitoid responses within colonies mediated by alarm pheromone, (E)-β-farnesene) (Hatano, Kunert & Weisser, 2010). There is no other way that one organism can convert into another without change at the population genetic level, dependent on changes of gene frequencies in that population under selection. Ultimately, assuming the evolved population has favourable characteristics, it and its associated genome may become ‘fixed’ within the new population in question and perhaps even dominant (Coyne & Orr, 2004). This evolution of new forms has to go through several ecological steps involving various population mechanisms leading to divergence. These include population restriction events (new invasions, bottlenecks), geographical separation (islands, metapopulations) and behaviour, often with the formation of intermediate forms on the path to full speciation (Ayala, 1978; Ridley, 1993). The arising modified population must have some advantage and adaptation that allows it to differentiate and thrive in novel ecological situations. Ultimately, it becomes a new biological entity occupying n-dimensional space in relation to a plethora of abiotic and biotic factors (Hutchinson, 1959). This state is unique to each and every organism on the planet, even subspecific forms that may inhabit widely divergent habitats from the original parental stock from which they evolved (e.g. British butterflies; Riley, 2007); it accounts for the geographical distribution of closely-related organisms, sometimes overlapping or parapatric, such as nuthatches (Sitta spp.) (Zink, Drovetski & Rohwer, 2006). In effect, speciation involves ecological specialization and vice versa. The two are inseparably bound, which means that, if generalization or ‘generalism’ as it is usually termed exists (at its most fundamental level, associated with polyphagy; see the subsection ‘Food’ in ‘Mechanics of Adaptation’ below), it must be some kind of niche specialization, perhaps broad, but nevertheless a specialization. The huge biodiversity of extant taxa on Earth today (approximately 1.9 million species), especially insects (estimated at approximately one million species), in addition to all the extinct taxa that once existed over vast swathes of time (Grimaldi & Engel, 2005), is testament to this fact. What the exact nature of many, if not most, of these extinct niches was exactly, we will doubtless never know (also, on a more philosophical note, do niches really exist or are they created by the organisms concerned?; Polechová & Storch, 2008); whatever, the procession of different life forms down the ages has surely involved ecological specialization of one form or another, often very tight.

To be maintained, this kind of divergence must not only involve barriers to mating and reproduction, but also it must be beneficial and allow the new habitat and resource to be exploited. A crucial aspect of this is that intraspecific competition between the novel and original populations is offset in some way in terms of fitness. This divergence mostly comes about by habit specialization, although there are examples where sudden chromosomal changes preclude mating between previously sympatric and contiguous populations (White, 1978). However, sometimes divergent populations may come back together again at hybrid zones and population mixing and the production of fertile hybrids may then occur (Barton & Gale, 1993; Rieseberg, 2001; see below).

Thus, if habitat adaptation (i.e. specialization) is the cutting edge of evolution, how can so-called ‘generalism’ be maintained in an evolutionary sense? Indeed, does generalism actually exist in nature, or is generalism a function of ‘time slice’ observations (Loxdale, 2002) and the associated degrees of resolution within a study? Accepting that ecological specialization is the main driving force leading to speciation, then it may perhaps be stated that evolution has a direction (i.e. analagous to time) that is always a forward one; for example, Dollo's (1890) ‘Law of Irreversibility’ named after the famous Belgian palaeontologist Louis Dollo (1857–1931), in which organisms tend toward fine tuning with their habitats, including morphology, niche specialization, fidelity and, most importantly, food resources. This is also a point broadly emphasized by the equally famous American palaeontologist Edward Drinker Cope (1840–97) in his book The Primary Factors of Organic Evolution (Cope, 1904; originally published 1896) where he states (p. 75) that ‘The study of phylogeny shows that the evolution of life-forms has been from the simple to the complex, and from the generalized to the specialized’. Later (p. 175), he talks about the ‘Doctrine of the Unspecialized’, which describes the fact that ‘the highly developed, or specialized types of one geologic period have not been the parents of the types of succeeding periods, but that the descent has been derived from the less specialized of preceding ages’. So, although he considers that generalist and specialist entities exist in nature, he also assumes in a neo-Lamarckian way that biological complexity (progressive evolution) derives from more generalist life forms via a process analogous to the inheritance of acquired characteristics (for further discussion, see Bowler, 1977).

To return to our modern day understanding of the topic, even intrasexual competition and sexual selection tends to drive animals towards increasing specializations of behaviour and form, which increase the fitness of those that indulge in such scenarios, although there are also ‘trade-offs’ in longer-term individual and species survival. Nevertheless, these latter selection mechanisms, which often lead to elaborate barriers to further adaptive radiation, do not necessarily lead to further speciation.

When trying to assess the reality of the phenomenon of generalism, we wish to put forward the idea that it cannot be maintained over the longer evolutionary term. Although generalism (which may anyway be seen as a spectrum rather than an extreme state) may have short-term benefits to the individuals and populations concerned, selection will inevitably mould these towards greater degrees of specialization. We wish to show that, even for animals that appear to be generalist, these are to some extent (usually greater) specialist in terms of habitat and resources. One could state that if one accepts the theory of evolution, involving as it does population divergence and adaptation, can generalism be accepted as anything more than a passing phase in certain species evolutionary scenarios? In this reappraisal, we do not discuss plants in any detail, nor the various mechanisms leading to evolutionary divergence in animal and plant populations because these are described elsewhere (Mayr, 1963; Dobzhansky et al., 1977; White, 1978; Ridley, 1993; Rieseberg, 2001; Coyne & Orr, 2004). Instead, we focus on data supportive of the universality and importance of specialization as the quintessential evolutionary driving force and contrast these with examples purporting to show generalism, especially with reference to insects, our own speciality.


  1. Top of page
  2. Abstract

Erroneously, Lamarckism encompasses a change of morphology, etc. in a short period of time (thousands of years), brought about by environmental feedback (Browne, 2003; Loxdale, 2010a). By contrast, evolution as originally espoused by Charles Darwin (1809–82) (later termed ‘Darwinism’ by Wallace, 1889) describes the selective processes of evolution over a geological time scale (Origin of Species; Darwin, 1859). In his later book, Variation in Plants and Animals under Domestication (Darwin, 1868), Darwin began to consider and incorporate Lamarckism in some form (e.g. Pangenesis) because he noted evolutionary changes over short periods, such as in the selective breeding of domesticated animals. This period may thus be described as a dilution of his original decisive statements concerning the mechanisms of evolution involving natural selection. Whatever, Darwin ultimately came to terms with a state of change much more dynamic and occurring within a single human observer's lifespan.

Evolution is, even today, generally perceived as a slow process, although it has been definitely shown to occur rapidly, as elegantly elucidated by Thompson (1998) and Rieseberg (2001) (for insects, see also Loxdale, 2010b). Examples are now known of several steps to full speciation, leading from ecotypes, biotypes, strains, races, and, subsequently, to sibling, sub- and full species (Ayala, 1978; White, 1978; Claridge et al., 1997; Loxdale, Claridge & Mallet, 2010). Regardless of the debate concerning the definitions of species and the processes involved (e.g. the biological species concept), all true species have a degree of reproductive isolation, spatial, and/or temporal (Claridge et al., 1997; Kunz, 2002; Ortiz-Barrientos & Rieseberg, 2006; Claridge, 2009; Foottit & Adler, 2009). Over the short time scales in which evolution has been directly observed, such changes occur at the subtle molecular through to chromosomal level, rather than necessarily involving morphological differences (Rieseberg, 2001), although rare examples are known of fertile hybrids between ‘good’ species. Excellent examples include the famous Peloria named by Carl Linnaeus (1707–78) in 1742 (meaning ‘Monster’ in Greek) for a mutant form of common toadflax, Linaria vulgaris Miller (Coen, 1999) and the intraspecific hybrids between sunflowers, Helianthus spp. (Ungerer et al., 1998) and Lycaenid butterflies, Lycaeides spp. (Gompert et al., 2006, 2008), respectively, all of which do involve morphological change.

Agricultural and medical–veterinary systems are the best areas exemplifying rapid evolution. Classic examples in these systems include: plant-host resistance breaking genotypes in biotypes of the greenbug aphid, Schizaphis graminum (Rondani) (Hemiptera: Aphididae) (Puterka & Peters, 1990; 1995), pesticide resistance in the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), including to Bt (Bacillus thuringiensis) toxins (Tabashnik, 1997); prophylactic resistance in Plasmodium spp. (Imwong et al., 2010); and antigen variation in trypanosomes (Morrison, Marcello & McCulloch, 2009).

In these particular cases, it could be argued that speciation in the strict sense has not occurred, and that these are merely strain variations below the species level. Even so, there are examples within natural populations in which sudden chromosomal changes occur, such as translocation events leading to instant speciation, both within sexual and asexual organisms (White, 1978; Coyne & Orr, 2004; Schön, Martens & van Dijk, 2009). Normally, species divergence occurs at the population genetic level involving the entire genome. African cichlid fish (Young, Snoeks & Seehausen, 2009) and European house mice (Mus musculus L.) populations display this form of rampant evolution (e.g. the so-called tobacco mouse; Hauffe et al., 2004), also aided by transport by humans in the case of mice (e.g. by the Vikings; Searle et al., 2009). In insects, which often have fast rates of reproduction, rapid evolutionary changes (morphological, chromosomal–genetic, chemical–biochemical, and behavioural) are now well established, including below the species level, often starting as ecological specializations (Loxdale, Claridge & Mallet, 2010). A good example of this phenomenon is the ecological specialization of the pea aphid, Acyrthosiphon pisum (Harris), on a range of leguminous hosts in which largely reproductively isolated host-adapted forms have been found, which in turn are associated with the bacterial endosymbiont type (Knäbe, 1999; Peccoud et al., 2009; Peccoud & Simon, 2010).

One of the mechanisms instrumental in bringing about these rapid changes is that of co-evolution (Thompson, 1994). Thereby, it is found that organisms are not evolving independently, in the ‘absence’ of other organisms, but rather they co-evolve in an antagonistic (i.e. adapting to selective forces such as predation and parasitism) or, more rarely, mutualistic fashion (e.g. pollination). This phenomenon occurs across all trophic levels with different levels of benefit and fitness trade-offs to the co-dependents (for aphid bacterial endosymbionts, see Moran, 1996). These dependencies are often very intimate, such as beak length in hummingbirds and tongue length in bumblebees and moths in relation to flower trumpet length (for bumblebees, see Goulson, 2009). With predators and parasites/parasitoids and their prey/hosts, co-evolution could take the form of defence mechanisms, including avoidance behaviours, such as the response of aphids to alarm pheromones (Pickett & Glinwood, 2007). With plants, co-evolution could similarly involve defence (anatomical or chemical) or even behavioural (mimosa leaves closing on contact) responses (Thompson, 1994; Freeman & Beattie, 2008). Sometimes, specialisms include very intricate behaviours and examples are to be found in bees. The nesting of solitary bees (Family Megachilidae) in snail shells, nest design and decoration in Mason bees (Osmia spp.), and pollen selection in bumblebees differentiating between flower species through to families are all examples. Many specialists such as parasites or butterflies specialize on closely related taxa (families, genera, etc.). Lastly, the co-evolutionary scenario could involve mimicry, cryptic, Batesian or Müllerian. In the case of the latter two mechanisms, where some detriment occurs to one of the partners, an ‘arms race’ may be elicited in which the organism under threat attempts to evolve away from that threat. The classic example in mimicry concerns the model evolving away from the mimic, which appears to be parasitic upon it (a case of ‘identify theft’, to use the modern parlance; but see also Rowland et al., 2007 and Hanifin, Brodie & Brodie, 2008). Other parasitic insects such as fleas (Order Siphonaptera) show various species dependent levels of polyphagy, although host synchrony and location is always likely in the longer term to drive less co-evolved kinds towards adaptations (Rothschild & Clay, 1952; Rothschild & Ford, 1969). In some parasites, such as Trypanosomes, co-evolution of immune responses (in effect, a molecular arms race) tends to make them host-specific, although they can change host but then become seriously pathogenic (ultimately lethal) as a result of maladaptation (for Chagas disease, Trypanosoma cruzi, see Pérez-Fuentes et al., 2003). When the relationship is mutually beneficial, as with pollinator and pollinated, selection may also act quickly because the fitness of both is positively influenced, leading to a ‘tight’ relationship in terms of form, function, and often behaviour, including in butterflies (Mevi-Schütz & Erhardt, 2003). Certainly, in parasites, there is the necessity for a close synchrony in timing between co-evolved partners (Thomas, Renaud & Guégan, 2005). With all the aforementioned evolutionary scenarios, presumably equilibrium is reached at some point, when the evolutionary trade-offs between benefit and disadvantage are balanced. The co-evolution of herbivorous insects with their host plants and parasitic insects with their insect hosts, with insects representing 75% of all animals on Earth (Grimaldi & Engel, 2005) and a group on which much new work has focussed concerning co-evolutionary trends and mechanisms, is discussed in more detail in the section ‘Co-evolution’ below.


  1. Top of page
  2. Abstract


Adaptations, whether they be specialized or more ‘generalist’, are predominantly associated with food (mono-, oligo-, and polyphagy) but, concomitant with the quest for its acquisition, are behaviours, including types and patterns of mobility, that have a bearing on how adaptations are maintained. The core feature of specialism is food resources. Within a niche, a successful form may begin to outgrow the available resource and, in such a situation, intraspecific competition is always likely to occur. There are many scenarios where such limitation is overcome. This is usually embodied in the individual's quest for resources by exploration away from the ‘fixed’ niche, although it could involve co-operative ‘bodies’ such as army ants (e.g. Eciton burchellii Westwood), which pool their efforts by a caste-defined hierarchical social framework. Notably, such eusocial insects are exceptional cases and have their peculiar evolutionary advantages and disadvantages (for a detailed discussion of the morphological, chemical, behavioural, and ecological specializations of ants, including in terms of food resources, see Keller & Gordon, 2010). In addition, populations undergo a spatial and temporal demarcation of resources. Animals may be after the same food but start to develop adaptations, perhaps behavioural or anatomical, that cause the organisms concerned to diverge in terms of exploitation of the ecosystem. For example, in bushbabies (Galagos), some previously assumed ‘good’ species forage at different strata within the forest canopy, although it has now been shown that these include cryptic species, separable on various criteria, including vocalizations, morphology, and mitochondrial DNA (Honess & Bearder, 1997; Bearder, 1999). Some species (e.g. monkeys) may be active at night or day, when they pursue and eat essentially the same food items. By way of contrast, forest communities of the Chimpanzee, Pan troglodytes Blumenbach, although appearing to have both specialist and generalist dietary foraging tendencies (Newton-Fisher, 1999), are essentially ripe fruit specialists (Wrangham, Conklin-Brittain & Hunt, 1998). Within the same species, however, or at least within a homogeneous species population, few individuals have drastically different behaviours for food acquisition. There are exceptions to this (e.g. Leopards Panthera pardus L.) and, again, these could be precursors of specific adaptations (Johnson et al., 1993; Bothma, 1998). In addition, one is reminded of the now extinct Huia bird, Heteralocha acutirostris (Gould) of New Zealand whose sexes had different bill morphology (size and shape) and apparently slightly different food preferences, and thus in some respects, differing ecologies (Fuller, 2001).

Although many mammalian herbivores appear to be generalist grazers or browsers, they are in fact limited by adaptation to specific vegetation types (e.g. grazing, bushes, etc.) and, within those, may be specific in terms of food preference to a greater or lesser extent (for grazing cattle, see Ganskopp & Cruz, 1999).

A lack of habitat and or host/prey fidelity appears to be a requisite for generalism [for insects, see Novotny et al., 2002; 2006; Novotny & Basset, 2005; see also Novotny et al., 2006: figure 2, where most species of folivorous insects (Lepidoptera, Hymenoptera, Coleoptera, and Orthopteroids) surveyed on trees, both in the tropics and temperate forests, are clearly specialists]. Presumably, this is matched by suitably expansive behaviour and the ability and will to move between resources and resource patches (i.e. opportunism). As is known in species that apparently show sympatric adaptations, pre-mating host preferment and chemical attraction, as well as allochronic differences between insects on different suitable hosts, tend to reinforce host associations, as found in Rhagoletis fruit flies (Diptera: Tephritidae) (Feder, Berlocher & Opp, 1998; Linn et al., 2003; 2004; Feder & Forbes, 2010). Again, in insects, sap suckers are more likely to be polyphagous than chewers because the phloem is less subject to the host production of antagonistic secondary plant chemicals than the plant tissue (but see also Novotny & Basset, 2005 who claim that both groups are equally specialist, approximately 56% of species examined). Having the right array of detoxifying enzymes (with specific allosteric binding sites) is the key to polyphagy and, because of its presumed expense (Berenbaum & Zangerl, 1994; Agrawal et al., 2002), many species opt for co-evolved relationships and only detoxify or sequester the antifeedant chemicals of one plant family or genus; for example, the viceroy butterfly, Limenitis archippus (Cramer) (Nymphalidae), whose larva is protected by sequestered nonvolatile defensive compounds (phenolic glycosides) from its host plant, Carolina willow, Salix caroliniana Michaux (Salicaceae; Prudic et al., 2007); swallowtail butterfly larvae, Papilio spp. feeding on plants containing furanocoumarins which they can detoxify (cytochrome P450 monooxygenases; Wen et al., 2006; Mao, Schuler & Berenbaum, 2007); and mustard oils (glucosinilates) by mustard aphids, Lipaphis erysimi (Kaltenbach), via the enzyme myrosinase (but see also Bridges et al. 2002). In the case of aphids, even if the species is apparently polyphagous during the asexual summer generations, the necessity for males to ‘home in’ on sexual female sex pheromones probably limits the number of primary woody hosts used on which overwintering eggs are laid in many host alternating species (Pickett & Glinwood, 2007). Furthermore, many aphids, when returning from secondary hosts on which they may be more or less specific (e.g. infesting one family of plants Cruciferae or Gramineae), are very specific in terms of the overwintering woody host, often a single member of the Rosaceae (e.g. peach, Prunus persica, in the case of the peach-potato aphid, Myzus persicae (Sulzer); Blackman & Eastop, 2000). Perhaps in highly polyphagous aphid species such as M. persicae (reputedly attacking secondary host plants in 40 different families, including many important economic crop plants; Blackman & Eastop, 2000), general detoxification enzymes, especially including carboxylesterases (Devonshire, 1989), allow the insect to exploit a wide range of plant host species, many with secondary plant toxins such as alkaloids, as found in potatoes and deadly nightshade Atropa belladonna L. (Solanaceae). Again, how much of the toxin (the alkaloid atropine in A. belladonna) is imbibed via the phloem is not clear and may be much less than a chewing insect would encounter. Furthermore, perhaps the range of toxins encountered have structural similarities, allowing them to be detoxified by relatively few enzyme systems. Lastly, in the case of M. persicae s.l., one might reasonably ask how many of these various plants is the aphid truly generalist on? Already two host specialists are known: Myzus persicae nicotianae (Blackman) on tobacco (Blackman, 1987) and M. antirrhinii (Macchiati) on snapdragon, Antirrhinum spp. (Hales et al., 2000), which have unique chromosomal numbers/and or genotype banding pattern profiles (ffrench-Constant et al., 1988), and, in the tobacco aphid, behavioural/sex pheromone aspects of the life cycle that reinforce specialism (Margaritopoulos et al., 2007). Surely other host adapted forms of this species await discovery (see Co-evolution section).

Because of the nature of plant secondary compounds, herbivores will always be limited in the range of species that they can eat, whilst anatomical defences (spines, stinging hairs, etc.) are also likely to discourage unadapted ‘generalists’. Even mutualistic leaf cutting ants (Atta and Trachymyrmex spp.) specialize to some degree in having preferred hosts (i.e. dicots) (Nagamoto et al., 2009) and behaviourally avoid unpalatable plants or parts of plants that may inhibit their fungal gardens or are expensive to cut (i.e. old leaves) and which may thus lower the ant's fitness (Seal & Tschinkel, 2007; Mundim, Costa & Vasconcelos, 2009). The ants themselves do not eat the plants but only imbibe its nutrients via an intermediary organism (Keller & Gordon, 2010).

With true predators (as adverse to insect endoparasitoids that devour their host internally, finally killing it), flesh is flesh and if the prey falls within the prey size range of the predator, it is likely to be predated, assuming that no specific defences are present to dissuade the would-be attacker, including toxins (as found in shrews). Many poisonous animals are apparently immune to their own toxins or that of closely-related organisms (e.g. snakes: Hoser, 1985; scorpions: Shulov & Levy, 1978), whereas some predators that prey on poisonous creatures such as the European hedgehog, Erinaceus europaeus L., attacking venomous snakes, are partially immune to their venom (Omori-Satoh et al., 1998). Hence, these evolved attributes amount to a highly degree of adaptive specialism. Spiders that spin webs to collect flying insects may appear to be generalist, although the type and size of prey must to a large extent be determined by location of the web within the ecosystem and prey size: stronger, bigger insects are more likely to escape before being trussed up and paralysed and communal activity thus helps the spiders tackle larger prey. Such a situation is seen in the social theridiid spider, Anelosimus eximius Keyserling of Panama, which catches an unusually high number of large insects; some 90% comprise flying ants, beetles, lepidopterans, hemipterans, cockroaches, and grasshoppers (Nentwig, 1985). Many parasitic insects appear to be generalist (e.g. parasitic hymenoptera; Godfray, 1994) but, here, co-evolution with the host in terms of host location and emergence synchrony is likely to lead to specializations, and many apparent ‘good’ species are either wrongly identified or are cryptic specialists (see the section ‘The Problem of “Time-Slice” Ecology’ section below). In addition, the fact that some species such as braconid parasitoids (Hymenoptera) attacking aphids use chemical cues (kairomones) from the ‘mummy’ case (exoskeleton of the aphid host in which the parasitoid pupates), when they emerge as winged adults to locate the plant host from which their original host came, is likely to reinforce specialization (Storeck et al., 2000). Some parasitic wasps of moths are very host specific, only attacking very closely-related species, again probably as a result of life-cycle synchrony and chemical cues (Janzen et al., 2009). It is certainly well established in studies of agricultural pests and so-called beneficial insects that tobacco, maize, and cotton emit volatile substances (semiochemicals) when damaged by the caterpillars of certain moth species that allow wasp parasitoids to locate these food resources (De Moraes et al., 1998; Rose, Lewis & Tumlinson, 1998; Paré & Tumlinson, 1999). That specialist parasitoids can differentiate between caterpillar hosts (De Moraes et al., 1998) suggests that, over time, this scenario has led to a high degree of behavioural-ecological fine-tuning in such complex tri-trophic systems.

Most carnivores are specialists in the range of prey taken (although there is often overlap; Lanszki et al., 1999). Thus, for example, wild cats, Felis sylvestris Schreber, although appearing generalist (i.e. consuming 28 species including birds' eggs in a study in south-eastern Spain), are, depending on location and time of year, largely specialists, with mice and voles predominating in their diet (> 80–90%; Moleón & Gil-Sanchez, 2003). Nonsuburban red foxes (Vulpes vulpes L.) predominantly predate roe deer, Capreolus capreolus L., and voles along with other small mammals, with which they have co-evolved as hunter and hunted (O'Mahoney et al., 1999). In Israel, the diameter of the canine teeth of sympatric small wild cats is non-overlapping depending on prey size (Dayan et al., 1990), indicating these animals too have evolved specific morphological features associated with lifestyle/diet. Probably, these predators exploit the most abundant and easily accessible food resource available at any one time and place and are thus highly opportunistic. However, in the insect world, ladybird beetles (Coccinellidae) appear to show definite aphid host preferences and preferentially lay eggs on the plant hosts supporting their favourite species (Omkar, 2005). When such host preferences evolve, if subpopulations become isolated in a genetic sense (e.g. chromosomal inversions or gross karyotypic changes), as well as a reproductive sense, for whatever reason, then specialisms may start to develop when regionally or temporally abundant food items are available.

Co -evolution

As noted above, many organisms involved in intimate interactions, such as herbivorous insects and their food plants, exhibit phenotypes based on long periods of co-evolution between them. Indeed, the process of co-evolution constitutes a long-standing foundation in our understanding of plant–insect interactions (Ehrlich & Raven, 1964; Fox & Morrow, 1981; Jermy, 1984; Bernays, 1988; Futuyma, Keese & Scheffer, 1993; Janz, Nyblom & Nylin, 2001; Janz, Nylin & Wahlberg, 2006). Amongst the examples of interdependent specialist insect–plant co-evolutionary relationships, perhaps those of orchid bees (Tribe Glossini; Ramirez, 2009) and fig wasps (family Agaonidae; Cook & Segar, 2010) are the most well known. In these extreme mutualistic scenarios, the fitness effects benefit both partners. Even so, there are other scenarios where plants evolve defences that repel or deter insect herbivore attack, whereas the herbivores themselves evolve counter adaptations to deal with plant defences. Ultimately, this leads to an evolutionary arms race, whereas some measure of equilibrium is maintained between plant response to herbivory and insect-counter-response over time (Thompson, 1988a, b). Furthermore, such an arms race is predicted to lead to specialization in herbivore diet, leading to intimate associations between plants with phylogenetically-conserved chemical defences and certain herbivore lineages (Feeny, 1976). The larvae of butterflies in the family Pieridae, for example, feed only on plants in the order Brassicales that produce secondary compounds known as glucosinolates (Hopkins, van Dam & van Loon, 2009). These are detoxified by specialist adaptations, including enzymes such as myrosinases and a tandemly duplicated nitrile specifier protein, the latter hydrolysing glucosinolates to nitriles instead of the more toxic isothiocyanates and which is considered to have evolved in the last 10 million years or so (Wheat et al., 2007). As the levels of chemical plant defence increase, poorly adapted generalist herbivores are forced to either adapt locally to certain plant types or else to switch to plants with lower levels of allelochemicals (see below). This may explain why cropping systems are often inundated by apparent generalist herbivores. Artificial selection by humans has often been aimed at reducing foliar levels of defensive chemical compounds because these chemicals have a repellent taste (Gols & Harvey, 2009). Domesticated plants are effectively ‘disarmed’ and thus act as reservoirs for generalists that are otherwise rare on much more toxic wild type plants (Gols et al., 2008).

Another shortcoming in our understanding of dietary generalism in insect herbivores is that it is very often based on observations made at the species level. However, with increasing physiological scale from individuals to populations, the level of generalism exhibited within a species may increase quite markedly and vice versa. Consequently, insect herbivores that are considered to be generalists at the level of species may tend to be more specialized at the level of populations and even more so as individuals [for the larch and pine host races of the larch budworm moth Zeiraphera diniana Guenée, see Emelianov, Marec & Mallet (2004); for the putatively oligophagous Neochlamisus bebbianae (Brown) beetles (Chrysomelidae), see Funk (2010)]; in both cases, the host adapted forms show strongly differentiated gene loci despite gene flow, reflecting divergent host-race selection). Specific genotypes may also become locally adapted to the most common plant species found in a particular habitat. If certain plants are dominant locally, then this would be expected to lead to frequency-dependent selection for herbivores to adapt to these plants and to become specialists over time. Recent studies by Singer and colleagues (Bernays & Singer, 2005; Singer, Mace & Bernays, 2009) have begun to unravel the physiological mechanisms and adaptive significance underlying polyphagy in woolly bear caterpillars (Arctiidae). The mandibular sensilla of neonate caterpillars are very sensitized to the presence of certain allelochemicals, such a pyrrolizidine alkaloids or iridoid glycosides, in plant tissues. The presence of these compounds stimulates initial feeding bouts in these generalist caterpillars but, as the larvae accumulate these toxins, they become less receptive to them until they actually become repellent. This leads to dietary switching to plants with other kinds of secondary compounds (Fig. 1A). These herbivores are described as ‘specialized generalists’ because their feeding behaviour is innately programmed to prefer certain allelochemicals in different stages of their larval life-cycles. In another recent study, Dyer et al. (2007) show that the diet breadth of the caterpillars of temperate species is much broader than that of tropical species, which show greater degrees of host specialization. In effect, there is ‘greater turnover in caterpillar species composition (greater β diversity) between tree species in tropical faunas than in temperate faunas’. This is claimed to be a result of relative increased differences in terms of secondary plant compounds in leaves of trees species in the tropics compared to the temperate zone, as well as a higher and more diverse pressure from natural enemy communities.


Figure 1. A, conceptual diagram showing a possible route through which different populations of a generalist insect herbivore (in this example, the cabbage moth, Mamestra brassicae L.) may evolve dietary specialization leading to reduced gene flow amongst populations and eventual speciation. In this example, the herbivore attacks 3 different plant species in nature. Each plant species is unrelated and has evolved specific types of phytotoxins in response to selection pressure from herbivores, whereas the herbivores evolve counter strategies to avoid, sequester or detoxify the plant's chemical defences. Selection is strongest between the ancestral generalist herbivore (‘herbivore 1’) and plant species 1. Herbivores attacking this plant may develop ‘composite specialization’ whereby a specific genotype of this herbivore species may prefer this plant as an oviposition and feeding site over the other plant species. Preference may be based on adaptations to plant characteristics such as volatile emissions, architecture, the presence of enemy-free space and alleochemistry. In time, adaptation to this plant and possible reproductive isolation (e.g. where the frequency of local mating is strong) may lead to oligophagy in this herbivore. Composite specialization has been observed in a number of lepidopteran herbivores (see text), and there is abundant data showing that some herbivores considered as ‘generalists’ are very choosy in their feeding habits. B, possible pathways leading to specialization in parasitoid wasps. Here, the larvae of the cabbage moth, Mamestra brassicae, are suitable for the solitary endoparasitoid, Microplitis mediator Haliday, whereas larvae of the large cabbage white butterfly, Pieris brassicae L. are not, even though both herbivores are abundant in cabbage crops. The composition of herbivore-induced volatile profiles has been shown to vary both within and between different plant species, even to the level of the attacking herbivore. Parasitoids may evolve responses to certain odour blends (light grey and dark grey ‘clouds’; Nb. green and grey on the online version) associated with specific herbivores; at the same time, given that different herbivore species may deal with ingested plant toxins in a species-specific manner, this may drive endoparasitoids to restrict their development on hosts with specific physiological mechanisms in dealing with these toxins (see above). Furthermore, immunological defenses in herbivorous insects are phylogenetically conserved, meaning that endoparasitoids may evolve counter mechanisms targeting a very limited range of host taxa. These mechanisms may involve specific venom proteins, polydnaviruses, virus-like particles, and bacterial symbionts that regulate host immunity and development in ways that are association-specific.

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Parasitoid wasps are also good subjects for studying the switch from generalism to specialism (Fig. 1B). Parasitoids are involved in strong co-evolutionary arms races with their hosts, and are under strong selection to exploit the often limiting resources contained in individual hosts. Many parasitoids lay their eggs into the host haemoceol: these species are usually koinobionts, which are defined as parasitoids that attack hosts that continue feeding, growing, and defending themselves for variable periods after parasitism (Sequeira & Mackauer, 1992; Harvey, 2005). The eggs and larvae of endoparasitic koinobionts must cope with a potentially hostile and dynamic environment. Parasitoid eggs and neonate larvae must avoid the host's immune responses, which involve clotting, phagocytosis, encapsulation, and the production of antimicrobial substances. In most insect taxa, these defences are known to be phylogenetically-conserved, and they have been well-studied in host–parasitoid systems (Strand, 2008). Furthermore, many parasitoids are susceptible to differences in the quality of the host diet through the ingestion of toxic plant allelochemicals that may be sequestered by the host (Ode, 2006). Allelochemicals are also diverse, and exhibit strong phylogenetic conservation, meaning that parasitoids may need to adapt themselves to both host- and plant-related traits (Harvey, 2005). Many koinobiont parasitoids are known to regulate host growth, development, and behaviour through the injection of biochemical factors, including polydnaviruses, virus-like particle, venoms, and teratocytes that function in an association-specific manner (Vinson & Iwantsch, 1980). Individually or in synergism, all of these factors have driven the evolution of specialism in koinobionts such that most endoparasitoids are known to attack one or only a few closely-related species of hosts in the same families (Quicke, 1997).


During range expansion, the other restrictive factor is reproduction. For most organisms, survival and reproduction, whether sexual or asexual, involves individual interaction. The individual may accrue benefits by being in a social group or subpopulation, inclusive of food acquisition, but, ultimately, it is only an individual's genes that pass to the next generation in the light of selection (Dawkins, 1989). During that struggle to survive and reproduce as individuals, the organism in question, whatever its situation with regard to co-evolutionary trends, is competing directly with members of the population of its own species. They are the organisms that are most directly competing for immediate resources. Any evolutionary change that reduces this selective pressure is likely to be favoured and lead to novel adaptations. Other types of intraspecific selection, such as sexual selection (Darwin, 1871), may improve the fitness of males of the species but, as mentioned earlier, are unlikely to lead to population divergence.

With regard to populations, even apparently homogeneous species need to be considered in terms of their genetic variation. Often populations are found to be genetically discontinuous, either as a function of geography, usually latitude or longitude (e.g. clines) and, more rarely, as a function of sympatric causes. When populations are examined in detail, both spatially and temporally, genetically distinct subpopulations may be found at various levels of evolutionary divergence. Such populations often show the beginning of partial or complete reproductive isolation, depending on how much time has elapsed and how much adaptation has occurred since the forms separated. When these distinct forms are brought into contact, as in hybrid zones, then sometimes maladaptive forms may arise that reinforce population separation (White, 1978; 1985).

Life-cycle strategies are a remarkable adaptive specialization that allows a population to exploit different niches, resources, and apply concomitant reproductive strategies within these. Good examples are found among aphids that have sexual and asexual alternation of generations (Moran, 1992), often involving host changes over time (approximately 10% of species physically change plant host species between autumn–winter and spring–summer seasons; Eastop, 1986). Evolutionary changes in aphids, by the production of obligate asexual lineages in species with host alternation or, more rarely, the occurrence of chromosomal changes such as changes in chromosome number (which may cause lethal nondisjunctions during meiosis when the offspring try and mate with the original parental population (Blackman, 1980; Blackman & Eastop, 2007; Loxdale & Lushai, 2007), lead effectively to ‘instant speciation’ events. Such forms are thus on the road to becoming a new species, given sufficient time, specific adaptations, and lack of gene flow. A good example here is the karyotype-related host-adapted forms of the corn leaf aphid, Rhopalosiphum maidis (Fitch) (Brown & Blackman, 1988), in which sexual forms have rarely been encountered (Blackman & Eastop, 2000).

In stick insects (Order Phasmatodea), chromosomal re-arrangements, including changes of ploidy/hybridization/de-activation of the genes controlling sexuality can also lead to enforced asexuality (Scali et al., 2003), in turn leading to successful invasion and the conquest of new plant hosts/habitats by such asexual forms/species, especially including marginal ones less favoured by the parental sexual species (see also studies of stick insects of the genus Timema; Schwander & Crespi, 2009). Chromosomal re-arrangements generally, in both sexual and asexual species, and including inversion polymorphisms (known to be caused by transposon hotspots), can induce reproductive isolation, even sympatrically, whereupon populations are cast into new ecological circumstances (or maybe), allowing new favourable mutations to accumulate, which reinforce local adaptations (White, 1978; Mopper & Strauss, 1998; Ortiz-Barrientos & Rieseberg, 2006; Noor et al., 2007; for a review in relation to vertebrate evolution, see also Fredga, 1977).

In insects, when mating is involved, because host plant fidelities are likely to reinforce adaptation to a few hosts, generalism must presumably have trade-offs against the finding and acquisition of a mate, more especially when visual and olfactory (semiochemicals) are involved, as with the Rhagoletis fruit fly complex (Feder et al., 1998; Linn et al., 2003; 2004). Voltinism in such creatures as the large heath butterfly, Coenonympha tullia (Edwards) (Wiernasz, 1989), and photoperiodic/ecophysiological responses in aphids such as the pea aphid, A. pisum (Smith & Mackay, 1990), and marine insects such as midges, Clunio spp. (Diptera: Chironomidae) (Kaiser et al., 2010), maintained by selection, also militate against generalism by encouraging local ecological specialization.

In largely or completely asexual insects such as aphids, although some species appear to have widespread dominant clonal genotypes as assessed using high-resolution molecular markers (the so-called ‘Brave-heart clone’ of Myzus persicae: Fenton, Woodford & Malloch, 1998; the generalist clone of the grain aphid, Sitobion avenae (F.), in France: Haack et al., 2000), these are largely confined to large-scale, intensively cultivated areas containing a very few crop types or varieties (brassicas, potatoes, wheat). By contrast, in less intensively cultivated regions, recent studies have failed to show dominant genotypes, including in S. avenae (Loxdale, Massonnet & Weisser, 2010). Similarly, laboratory-based performance experiments on M. persicae have failed to demonstrate the existence of generalist genotypes (i.e. general purpose genotypes; Vorburger, Sunnucks & Ward, 2003).

Lastly, although phenotypic plasticity too may be accepted as some form of generalism, then again, it is not yet known how often such plasticity has a genetic basis, and hence is under direct selection (Whitman & Ananthakrishnan, 2009).


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  2. Abstract

Were such instances of generalisms examined over a realistic evolutionary time scale (whatever that may be, and which could either be measured in years or even millions of years in a case-specific way), then all such examples could well be seen to be temporary apparent generalisms en route to full specialization involving distinct habitat and resource allocation(s) (Loxdale, 2002; 2010b).

Certainly, it is now clear that increasing molecular and chromosomal marker resolution is highly likely to reveal (or has already) much greater levels of specializations than hitherto imagined within apparently genetically- and ecologically-homogeneous species populations. For example, from a phylogenetic point of view, the recent use of mitochondrial DNA cytochrome oxidase I barcoding (Floyd, Wilson & Hebert, 2009) alone supports the contention of rapid evolution [parasitic Tachinidae (Diptera): Smith et al. 2007; parasitic Hymenoptera Smith et al. 2008].

Parasitic wasps represent approximately 20% of recorded insects (La Salle & Gauld, 1991; Feder & Forbes, 2010; see also Berenbaum, 2009). Generalists examined using DNA markers often comprise specialized cryptic species. For example, in Costa Rica, barcoding of 171 parasitic hymenopterous morpho-species gave an extra 142 species; of the 313 provisional species found, 95% were undescribed, whereas > 90% attacked only one or two lepidopteran host species out of more than 3500 species sampled (Smith et al., 2008). Similarly, in Diptera, Smith et al. (2007) barcoded 16 generalist morphospecies of Tachinid fly, splitting these into nine generalist species and 73 specialist lineages. The take home message is ‘The more molecular markers you use, the more specialist species you are likely to find’. This has potentially profound implications for the construction of ecological food webs. It also has profound influences on what a species is exactly because many good species are seen to be subject to introgression events, as found between the grain aphid, S. avenae s.s. and the blackberry-grain aphid S. fragariae (Walker) s.s. (despite both species having identical chromosome numbers (2n = 18) and sex pheromones), leading to novel specialized host adapted hybrid forms (Sunnucks et al., 1997; Loxdale & Lushai, 2007; Loxdale, 2008). In addition, Berenbaum (2009) makes the point concerning the huge problem of synonymies within various insect taxa (‘30% of named species are illusions!’). As she states, the failure to recognize cryptic forms can result in insect pest management failures. Only when correct specialist parasitoids are identified can the system work effectively.

With extreme specialization, besides the threat of extinction if specialized niches close, or effective population sizes are drastically reduced leading to inbreeding depression and all the other supposed concomitant ills of inbreeding – for example, in the case of the Glanville fritillary butterfly, Melitaea cinxia (L.) (Saccheri et al., 1998), forms can emerge that are also specialized in other ways (e.g. size, shape, behaviour, and movement). Examples could include baleen whales, giraffes, lions, and sloths, respectively.

Genetic variability may be directly associated with specialization. Species populations living in heterogeneous environments tend to have more heterogeneity than those living in more homogeneous ones. Concepts of ‘diversity webs’ refer to this: thus, the central or core population has the most diversity (for hymenopterous parasitoids of aphids, see Nĕmec & Starý, 1984; Powell, 1994). As subpopulations diverge genetically and inhabit new niches and exploit new resources (e.g. an insect moving from an existing long-term host association onto a new host species such as fruit flies of the Rhagoletis complex host shifting onto new hosts plants, such as from hawthorn, Crateagus spp. to apple, Malus spp. (Rosaceae), in turn tracked by their braconid wasp parasitoids, Diachasma spp.; Feder & Forbes, 2010], then the arising population is likely to have a subsample of the available variation. In effect, this process is tantamount to a founder event(s). At the same time, such host shifts in theory allow for escape into ‘enemy free space’ (Jeffries & Lawton, 1984), with all that this means in terms of reducing interspecific competition, as well as escape from natural enemies (although apparently not in the immediately aforementioned case concerning Rhagoletis spp. and their specific parasitoids; for details, see Feder & Forbes, 2010). The radiation of populations from a historical area into new areas by a ‘stepping stone’ process of colonization and adaptation is also sometimes associated with a loss of genetic variation as populations spread outwards (Stone & Sunnucks, 1993). Thus, as they lose variability, the founder populations are, if anything, becoming more specialized, and have less plasticity in a genetic sense enabling them to exploit new ecological circumstances, should these arise.

The lack of genetic homogeneity within and among apparent homogeneous species populations can only be rigorously tested using molecular markers (i.e. DNA), and the degree of subpopulation resolution is in turn subject to marker choice, markers such as single-nucleotide polymorphisms and microsatellites tending to reveal much greater levels of genetic polymorphism than allozymes (e.g. in M. persicae, Wilson et al., 2002 using microsatellites versus Brookes & Loxdale, 1987 using allozymes). The use of such markers can lead to discoveries concerning subpopulation discontinuities, which may not otherwise be apparent, with a good example being asexual populations mixed with morphologically-identical sexual populations of insects (Sunnucks et al., 1997). Equally, they may reveal unsuspected host feeding preferences or confirm that apparent polyphagous organisms in reality comprise one or more host adapted forms.

Where generalists exist and, in many cases, their reality has yet to be confirmed with molecular markers or by other means, they may not be very specific in terms of their ecological structuring; that is to say, they can move between diverse habitats and feed on a variety of food articles. As described earlier, the use of high resolution molecular markers is bound to reveal cryptic species or lower forms of evolutionary divergence amongst morphologically-similar host species that appear to be polyphagous, including amongst aphids (Anstead, Burd & Shufran, 2002; Loxdale, 2008), and especially hymenopterous wasp parasitoids, whose taxonomy is fraught with problems of synonymy. There are numerous other examples. Even if the subpopulations were to merge and hybridize after a period of allopatric separation, the specialist group may have some competitive fitness advantage (as with insecticide resistance, also in aphids; Foster, Denholm & Devonshire, 2000), so long as that unique resource remains abundant or the selective agent (pesticides in the case of insecticide-resistant insects) is still used at an appropriately high level.

Putative generalists may have a competitive advantage in being able to exploit a range of niches and resources but, undoubtedly, resources have local abundances in time and space and some are of longer duration than others. Jaguars (Panthera onca L.) from South America predate fresh water turtles (Haemig, 2007), as well as other prey that they can more readily catch (larger mammals > 15 kg, comprising approximately 67% of the biomass consumed; de Azevedo, 2008). Because these big cats have the power to crush the shells of these reptiles, they can exploit a resource effectively excluded from other would-be turtle predators. Over time and if the predator derived enough fitness trade-offs by hunting turtles, it may be envisaged that the Jaguar would become specialized in tackling this food as a predominant part of its diet, as has the specialist Aardwolf Proteles cristata (Sparrman), a member of the hyena tribe (Family Hyaenidae: Subfamily Protelinae) that consumes mainly termites and other insect prey.


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  2. Abstract

Because the world is under continuing dynamic flux, today's abundant resources may become tomorrow's scarce ones. By retaining behavioural and ecological (niche and resource) plasticity, apparent ‘generalists’ retain the ability to transfer dietary allegiance to a new resource should this suddenly appear when the usual resource declines, which is a sceneario not open to the specialist.

Even so, the majority of animal species are specialists sensu stricto. Apparent or putative generalists only comprise a small proportion of taxa and there may be long-term evolutionary reasons as to why this is so. Seemingly, most generalists (or, at any rate, animals with broad diet ranges) are predatory, although generalist herbivores appear to exist, e.g. apparent polyphagous insect herbivores earlier alluded to and monkeys of various species. However, because of antifeedants, even these may specialize, such as Proboscis monkeys Nasalis larvatus (Wurmb), which preferentially consume certain types of young leaves (65.9%) and fruits (25.9%), of which > 90% involves the consumption of unripe fruit (Matsuda, Tuuga & Higashi, 2009). Clearly, the answer lies in the ‘balance sheet’ of fitness trade-offs and short-term gains in terms of resource flexibility, which cuts across resource allocation and patchiness within complex ecological systems. Many predators appear at low abundance within ecosystems, although omnivores such as starlings (Sturnus vulgaris L.) appear to be common enough. On the other hand, the larger, longer term picture suggests that speciation arises and indeed continues by processes very much governed by specialisms. Evolution could not work were organisms generalist (i.e. it would in effect stand still!). Hence, ecological specialization [LEFT RIGHT ARROW] speciation. If this is true, then it further suggests that generalism is an energetically costly and in some way flawed strategy, which is not common among the many scenarios found during the main thrust of biological evolution, or so it would appear. We posit the question: does generalism truly occur in nature and, if so, where? Or rather, is so-called generalism a mirage, an apparition that shimmers on the distant horizon but, on closer scrutiny, is found not to exist in reality? Is it because we have the term specialism that we feel duty bound as biologists to have the alternative term, in effect, to create a huge edifice that is in fact artifice?


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We thank Drs Sebastian Meyer and Nicola von Mende for enlightening discussions, and three anonymous reviewers for their constructive comments that have greatly improved the manuscript. We also wish to thank Tibor Bukovinszky for providing photographs of Mamestra brassicae and Pieris brassicae larvae and Microplitis mediator, and ©Entomart for the photograph of the adult and pupa of M. brassicae. This paper was originally given at the Royal Entomological Society (RES) annual international meeting ‘Ento 10’ held at Swansea, Wales, 26–28 July 2010. H.D.L. thanks the RES for providing travel and other funding enabling me to attend this meeting, as well as Professor Tariq Butt and Dr Miranda Whitten (Swansea University) for their kind invitations.


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